Research reportDecoding the representation of learned social roles in the human brain
Introduction
The need for social affiliation is central to normal human existence. Therefore, the act of social exclusion (or ostracism) practised across human societies and cultures and even by some non-human primates, is usually perceived as a powerful and emotionally distressful signal, even under very artificial circumstances such as a computer game (Williams et al., 2000). Being totally or partially socially excluded can lead the affected individual to try to conform or re-establish social links with the group (Williams et al., 2000), and to develop emotional preferences for partners with a higher tendency to include them (Andari et al., 2010). Functional imaging studies recording brain activity during experiences of social exclusion have revealed that the “social pain” experienced under these conditions seems to share neural substrates with physical pain, i.e., activations in right anterior insula, anterior cingulate, and lateral prefrontal cortex (Eisenberger et al., 2003; Masten et al., 2009; Sebastian et al., 2011). Intracranial electrophysiological recordings have also shown effects on theta power in insula and subgenual anterior cingulate cortex during the experience of exclusion (Cristofori et al., 2012). However, all of these studies were restricted to measuring activity directly while subjects experienced the exclusion situation. The underlying neural mechanisms of how people develop preference or aversion for partners following social interactions still remain largely unclear. Here, we explore the brain correlates of such learned social categorisations, using a modified version of the cyber ball game involving fictive partners with different profiles (includer/excluder). Previous behavioural studies have shown that in such a situation, normal volunteers quickly start to favour partners that included rather than excluded them, as measured by the number of ball tosses sent to those partners and various behavioural ratings such as trust and preference (Andari et al., 2010).
We tested the hypothesis that activity in the brain structures mediating the emotional reaction during exclusion would also carry information reflecting the learnt social categories when the involved partners are subsequently encountered in a context lacking explicit social or affective connotations. We measured with fMRI brain responses to different facial identities before and after a very brief social interaction (ball tossing game) with different partners. The analysis methods we used were based on pattern recognition (support vector classification) which predict from the subject's brain activity the face's social meaning as previously experienced in the ball tossing game (includer = “good”; excluder = “bad”; control face = “neutral”). This approach, often applied in other domains of imaging neuroscience for example to study perceptual representations (Haynes and Rees, 2006; Norman et al., 2006), is applied here, to our knowledge for the first time, to decode learned social attributes. Multivariate pattern recognition methods allow to differentiate between experimental conditions on the basis of the information present in the full pattern of activity across voxels and are therefore sensitive to distributed effects that may remain undetected by conventional mass-univariate mapping procedures testing only for circumscribed activation in- or decreases. In the present context, this approach permits to detect subtle changes in distributed activity patterns in regions of interest (ROIs) relevant for social emotion that arise with learning and discriminate between faces as a function of their learned social category.
Section snippets
Participants and fMRI acquisition
15 healthy young volunteers (11 male and 4 female aged 24.1 ± 3.8 years) were included in this study which had been approved by the regional ethics committee of Hôpital de Bicêtre, France. Functional images were acquired on a 3 T magnetic resonance (MR) system (Siemens Tim Trio) with 12-channel head coil as T2* weighted echo-planar image (EPI) volumes with 1.5 mm in-plane resolution. 33 transverse slices covering occipital, temporal and frontal lobes up to (ventral parts of) anterior cingulate
Behaviour
The social learning paradigm employed consisted of two rounds of ∼5 min of a modified version of the “cyber-ball” game (Williams et al., 2000) with two fictive partners (see Fig. 1B). FMRI data were acquired just before and just after playing the game. After completion of the whole experiment, subjects were asked to rate the four (during the two rounds) partners' behaviour along six different socially relevant dimensions (see Methods for the corresponding questions). The results of these
Discussion
In the current study, we investigated the brain correlates of learned social roles after a brief social interaction with fictive partners expressing different degrees of inclusion. Our results show that subjects discriminated the different social profiles, as confirmed by the ratings obtained for the partners along several socially relevant dimensions. Furthermore, the activity patterns of the includer (“good”) and excluder (“bad”) faces became more discriminable in the insula and the anterior
Acknowledgements
We thank Andreas Kleinschmidt for helpful comments on an earlier version of this manuscript. This work was supported by Centre National de le Recherche Scientific (CNRS) and Fondation pour la Recherche Medicale (AS and LM). This experiment was part of a general research program on functional neuroimaging of the human brain which is sponsored by the Atomic Energy Commission (Denis Le Bihan). We thank the NeuroSpin platform staff for their help.
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